Mite infestation in () in Israel – Characterization and Response to Treatment Horowitz, I.,1* Krupnik, S.,2 Bourdeau, P.,3 Landau, U.,4 Anglister, N.,1 Alias, R.1 and Zur, G.4 1 Zoological Center Ramat Gan (Safari) & Israeli Wildlife Hospital, 1 HaZvi Ave., Ramat Gan, P.O. Box 984, Israel. 2 Veterinary Clinic, 14 Rimon Str., Gealya, Israel. 3 Veterinary school - Oniris – Atlanpole 44307 , Nantes, France. 4 Koret School of Veterianry Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel.

* Corresponding author: Dr. Igal Horowitz DVM Dipl. ECZM (Wildlife Population Health), Zoological Center Ramat Gan (Safari) & Israeli Wildlife Hospital, 1 HaZvi Ave., Ramat Gan, P.O. Box 984. Israel. Tel: +972-3-6305318, Mobile: +972- 0544-650000, Fax: 00972-6305303. Email: [email protected].

ABSTRACT Hedgehogs (Fam. Erinaceidae) are among the most common in Israel. Their innate sensitivity to external and internal parasites can cause critical damage to their population that could create an imbalance of the ecological environment. Mite are common external parasites of hedgehogs and the current recommended treatment is the use of ivermectin. The hypothesis of this study was that hedgehogs are infested with mites in their normal state and in disease, however with a difference in the severity of infection depending on the hedgehogs' general health condition. The purposes of this study were (a) Investigation and characterization of mites infesting healthy hedgehogs captured in their natural habitat; (b) Characterize the disease caused by mites in clinically affected hedgehogs submitted to a wildlife hospital (IWH) and (c) to assess the success of treatment with ivermectin. Data were collected over a period of one year ( July 2011-July 2012) and included skin scrapings, microscopic examinations and fixation of mites for morphologic identification of mites' species. A disease severity scale was devised by the combination of clinical signs and microscopic examination of mites. Seventy hedgehogs were captured in their natural habitat, out of which 65 were not infested with mites and 5 were infested. Mite species were identified as Sarcoptes scabiei, Caparinia tripilis and one mite of the family Laelaptiae. Ninety three hedgehogs were brought to the Israeli wildlife hospital (IWH), out of which 48 were infested with mites identified as Sarcoptes scabiei. Thirty-four of the infested hedgehogs had dermatological signs only, suggesting that mange was not associated with any other internal diseases or injuries. No differences were found in the survival time of hedgehogs for the different degrees of skin disease, but survival rates dropped significantly during the first ten days of hospitalization, regardless of the severity of the dermatological disease. The release of hedgehogs back into the wild was made possible after 80-130 days of hospitalization, when their clinical signs had resolved. The significance of this work was the identification of the mite Sarcoptes scabiei as the most common mite species infesting hedgehogs in Israel and emphasizing that this species is a zoonotic parasite. Furthermore, to the best knowledge of the authors, this is the first report to describe the presence of a mite from the Laelaptidae family in a in Israel. The clinical importance of this study is in realizing that prognosis is not related to the severity of the dermatological disease. The critical days for survival are in the first 10 days of hospitalization.

Keywords: Hedgehog; concolor; auritus; Mites; Sarcoptes scabiei; Notoedres cati; Caparinia tripilis; Laelapidae; Mange.

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INTRODUCTION Table 1: Scoring system for mites infestation and skin problems Hedgehogs (Erinaceidae) are common mammals in Africa, 0 No mites, no clinical signs Asia and Europe (1). Mites are common external parasites 1 Mites in the absence of clinical sings of hedgehogs (2). Hedgehogs are very sensitive to external 2 Mites and appearance of alopecia and/ or itching 3 Mites and itching and/or crusts and internal parasites and this may lead to a decline in their 4 Mites and generalized skins lesions, crusts and itching population and cause an imbalance of the ecological systems (3). The mites that affect hedgehogs most commonly are: cording their data, which included estimated age, sex, weight, Caparinia tripilis, Sarcoptes scabiei, Notoedres cati (4, 5, 6). length, and after collecting skin samples, which consisted of Mite infestation primarily cause dermatological signs. skin scrapings from 3 regions from every hedgehog: ears, The clinical signs of mange are pruritus, lignification and nose and feet. crusts. The crusts are hard and thick and first visible in Data from affected hedgehogs that were brought to the areas such as the head, face and legs (7, 8, 9). In severe IWH between July 2011 and July 2012 were collected. All cases, dermatological changes extend to the rest of the were examined for their general health condition body and cause breakage of the spines from their and skin lesions. A scoring system for sick individuals was with resultant spine loss and as a result affected hedgehogs developed at the IWH (Table 1) and the affected hedgehogs often fail to roll up resulting in a loss of their protective were scored accordingly. The intensity of the infestation as ability, hypothermia and behavioral changes (9, 10). In well as the response to treatment was recorded. Skin scrapes were taken from all affected body sites. addition, the affected skin is often secondarily infected All skin samples underwent microscopic fixation and with bacteria (7). examination for mites and for their further identification. The current specific recommended treatment of hedge- The fixation was performed with Hoyer's medium (Dr. Yuval hogs for mites is Ivermectin (11). According to data from Gottlib Laboratory, Israel). the Israeli Wildlife Hospital (IWH), from 2010 there Treatment success with Ivermectin (Ivomec®, Merial, has been significant increase in the number of mange- Brazil) at a dose of 0.2-0.4 mg/kg body weight, per os (PO) affected hedgehogs that were brought to the hospital for or subcutaneously (SC) every 14 days for 3-5 treatments (8) treatment (Unpublished data, Personal communication: was assessed weekly and based on the clinical evaluation of Y. Horowitz). the hedgehogs and the detection of mites on microscopic There is a dearth of studies dealing with external parasites examination. Any dying during the course of treat- of hedgehogs and especially regarding their prevalence in the ment was recorded in relation to the severity of its disease wild population in Israel. This study planned to: (a) Examine condition. The treatment period until full recovery was the prevalence of mites on healthy hedgehogs captured in generally between 6 weeks to 3 months. their natural habitat and (b) characterize of the disease Statistical methods used to analyze data derived were caused by mites in clinically affected hedgehogs submitted Kaplan-Meier estimator and the Pearson’s test. Analysis was to a wildlife hospital (IWH) and (c) assess the efficacy of carried out using JMP 7 software (SAS Co.). Ivermectin for treatment. Mortality in the graph presented (Graph 1), is repre- sented by a decrease in the percentage of surviving hedgehogs MATERIALS AND METHODS relative to day zero. The recovery was set to the time when Two groups of hedgehogs were included in the study: wild the hedgehogs were released back into the wild. Length of hedgehogs that were captured in open areas in their natural time to release was conditioned on the absence of mites on habitat and sick wild hedgehogs that were transported to the skin scrapings and regrowth of spines and coat. In order IWH by individuals who found them. to properly present the effect of the treatment, only hedge- The first group of animals was captured between May hogs without related diseases were included. and September 2011, during the night. All captured animals All aspects of the study were approved by the Ethics were returned to their habitat after physical examination, re- Committee of the Hebrew University of Jerusalem, Approval

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Table 2: Data from the captured hedgehogs from the wild In order to estimate the effectiveness and the Males Females impact of Ivermectin treatment, the survival rate Species Total Young Mature Young Mature of hedgehogs in those animals, which were not Hemiechinus auritus 2 10 4 9 26 (37%) experiencing any concomitant disease, was exam- Erinacceus concolor 6 8 7 23 44* (63%) ined. The effect of the treatment with Ivermectin 8 (11.5%) 18 (26%) 11 (16.5%) 32 (46%) 70 was assessed by survival rate of hedgehogs that * p<0.05 (Pearson’s test) dermatologically were only affected with mange. No significant difference in the hedgehogs' No. MD-11-12901-2, and the Israeli Nature and Parks survival was found for the different disease severity degrees. Authority, approval No. 2011/38156. Over all, 19 of 34 hedgehogs survived (55.8%) (Graph 1). No significant difference in the hedgehogs' survival was RESULTS found for the different disease severity degrees; however, it was found that survival rates were low especially in the Seventy hedgehogs were caught in their natural habitats. first ten days, possibly as a result of stress caused from the Most of the hedgehogs (n=44) belonged to the species capture. Erinaceus concolor (63%) and 26 (37%) were of the species Hemiechinus auritus (Table 2). Sixty five individuals were free of mites and five were infested, and only one had skin lesions. DISCUSSION Sixty-six mites were harvested from the five hedgehogs These results indicate that only a small number of wild caught in their natural habitats. Fifty six (85%) were of the hedgehogs are infested with mites and those which are species Sarcoptes scabiei, nine (14%) Caparinia tripilis and infested usually showed dermatological signs without any one mite belonged to the family Laelaptidae. The number other medical issues. The presence of infestation with of mites found varied widely with 54 Sarcoptes scabiei mites Caparinia tripilis, without clinical signs, is not surprising isolated from a single one young male (Table 3). since the parasite has been described in the literature as In the second part of the study, ninety-three hedgehogs highly adaptive and living on the hedgehog's skin without were brought to the Israeli wildlife hospital during the causing any clinical signs (4). However clinical signs have study period, for various medical reasons. Each hedgehog been reported in a colony of African pygmy hedgehogs underwent a physical examination and its health status was in Korea infected with Caparinia tripilis, with clinical evaluated according to the scale from Table 1. Dermatological signs (12). This discrepancy may be explained due to an clinical signs were alopecia, yellow crusts, lichnification and increased sensitivity to Caparinia tripilis in African Pygmy broken spines. hedgehogs. Forty-eight hedgehogs (52%) were infested with mites. In one wild hedgehog a single hypoaspis mite from the The predominant species of mite was Sarcoptes scabiei (Figure Laelptidae family was found. In this family there are various 1). Caparinia tripilis was isolated from one hedgehog only parasites that are defined as obligatory or facultative parasites (Figure 2) and a mite from the Laelaptidae family was on of and . Their habitats are sandy soil as well one hedgehog (Figure 3). as nests of vertebrates and arthropods. This family has not yet

Table 3: Summary of findings for captured hedgehogs from the wild by species of hedgehog, sex, age, the number of mites found on each hedgehog and the species of mites present. Species of Hedgehog Sex Age No. of mites found on hedgehog Species of mites found E. concolor Male Mature 1 Laelaptidae spp. E hemiechinus Male Mature 2 Sarcoptes scabiei E. concolor Male Mature 6 Caparinia tripilis E. concolor Male Mature 3 Caparinia tripilis E. concolor Male Young 54 Sarcoptes scabiei

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Figure 1: Sarcoptes scabiei found on a hedgehog Figure 3: A mite from the Laelaptidae family found on one hedgehog.

this increase, including, public awareness for wildlife and for the possibility of available treatments, reduction in the natural habitat of hedgehogs due to increase in urbanization and increase in their proximity to humans. The fact that most of the hedgehogs were infested with Sarcoptes scabiei may also be the result of changes in lifestyle, contact to other species or interference with underlying causes resulting in decrease of defense and proliferation of the mites. Furthermore, Sarcoptes scabiei with its zoonotic potential could represent a risk for the people who are in close contact with the hedgehogs. Identification of the mites' species as Sarcoptes scabiei should raise awareness as this species is zoonotic parasite. Skin condition and the severity of the skin disease at Figure 2: Caparinia tripilis found on a hedgehog the clinical level do not appear to predict a failure or the success of the treatment. This result has significant clinical been described in Israel and in fact has not yet been described implications. The chances of survival of all hedgehogs are in hedgehogs at all. The ability to distinguish between dif- equal at first and the main obstacle is to survive the first ten ferent species of mites in this family is difficult, and requires days. Among all the hedgehogs there was mortality regardless the use a diagnostic tools in addition to morphology (13, 14). of the severity of the skin disease. At the clinical level it may The reason for the presence of these mites without clinical be stated that a hedgehog which survives the first ten days signs is unclear. has a greater chance for recovery. Recovery until release took The affected hedgehogs in the second part of the study, between 80-130 days, was dependent on re-growth of the consisting of those presented to the Wildlife Hospital, exhib- spines, as the hedgehogs without spines were unable to curl ited clinical signs consistent with those described in the liter- into a ball and to defend themselves, and therefore were unfit ature (4, 6). According to data from the IWH (not published, in the wildlife (4). Personal communication), in recent years there has been an More recently other treatments other than ivermec- increase in hedgehogs brought for treatment in general and tin have been described and demonstrated active against with mites' infestation in particular. Many reasons can cause Caparinia tripilis, such using the combination of moxidectin

20 Horowitz, I. Israel Journal of Veterinary Medicine  Vol. 75 (1)  March 2020 Research Articles Surviving

Treatment duration

Graph 1: Kaplan-Meier curve summarizes the percentage of hedgehogs caught in their natural habitats which surviving during the treatment with ivermectin until healing for the various levels of skin disease. Red – disease severity 2 (Presence of mites and appearance of alopecia and/or pruritis); Green – disease severity 3 (Presence of mites with pruritis and/or crusts); Blue – disease severity 4 (Presence of mites, generalized skin lesions and crusting). and imidacloprid (16) or the use of oral fluralaner, a recently REFERENCES launched isoxazolin (17). 1. Arbel, A.: The complete guide for Mammals in Israel. Publisher, Concomitant infestations have been described (17) how- Mapa. pp. 52-59, 2008. ever, it is unknown whether the presence of the two mite 2. Romero, C., Sheinberh Waisburd, G., Pineda, J. Heredia, R., Tarto, E. and Cordero, A. M.: Fluralaner as a single dose oral treatment species is with or without a synergistic potential having any for Caparinia tripilis in a pygmy African Hedgehog. Vet. Dermatol. clinical or other relevance. 28:622-e152, 2017. In conclusion, the significant findings of this work are 3. Perelberg, A. Scham, B., Dolev, A., Brenner C. and Kronveld- Schor, N.: A survey of mammals and reptiles on the coastal plain additional knowledge about mites infecting hedgehogs as a means of moving the animal breeding structure, important and treatment of infected hedgehogs. Identification of the definitions for conservation and a formulation of a plan for its foremost mites' species as Sarcoptes scabiei raises awareness preservation. Presented to the Department of Environment. Na- and the importance of this species as a zoonotic parasite ture Conservation Society, December 2006. 4. Brockie, R.E.: The Hedgehog Mange Mite, Caparinia tripilis, in (18), which must increase our mindfulness for methods of New Zealand. NZ Vet. J. 22: 243-247, 1974. prevention and control of these mites. Regarding treat- 5. Arlian, L.G.: Biology, Host Relations and Epidemiology of Sar- ment, the clinical importance of the prognosis seems to coptes scabiei. Ann. Rev. Entomol. 34: 139-161, 1989. have no connection with the severity of dermatological 6. Pantchev, N. and Hofmann, T.: Notoedric Mange Caused by No- toedres cati in Pet African Pygmy Hedgehog ( Albiventris). disease and recovery of the hedgehogs. The critical days Vet. Rec. 158: 59-60, 2006. in survival are during the first 10 days of treatment with 7. Robinson, I. and Roth, A.: Veterinary Care of the Hedgehog. In ivermectin. Practice. 21:128-137, 1999.

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